Calcium Ligation in Photosystem II under Inhibiting Conditions

Barry, Bridgette A.; Hicks, Charles H.; Riso, Antonio De; Jenson, David L.

doi:10.1529/biophysj.105.059667

Cited by 18 publications

(37 citation statements)

References 63 publications

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“…For example, our measurements are on a much faster time scale compared with rapid-scan Fourier-transform IR (FT-IR) studies of the OEC (for examples, see refs, [40][41][42]. Note that it has recently been suggested that a histidine perturbation may occur with S state cycling on the 10-s time scale (43).…”

Section: Discussionmentioning

confidence: 99%

“…The IR cell was assembled by using another calcium fluoride window and a 25-m spacer. The 25-m path length spacer was greased, and the sample was sealed with vacuum grease and parafilm to prevent dehydration during the experiment (42,49). A continuous-wave diode laser (Ekips Technology, Norman, OK) emitting at 1,483 cm Ϫ1 was used as the probe, a Q-switched Nd:YAG (neodymium:yttrium aluminum garnet) laser (Spectra-Physics) was used to produce a 532-nm photolysis pulse, and the transient absorbance of the probe was detected with a liquid nitrogen-cooled mercurycadmium-telluride detector.…”

Section: Methodsmentioning

confidence: 99%

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Time-resolved vibrational spectroscopy detects protein-based intermediates in the photosynthetic oxygen-evolving cycle

Barry

Cooper²,

Riso³

et al. 2006

Proc. Natl. Acad. Sci. U.S.A.

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Photosynthetic oxygen production by photosystem II (PSII) is responsible for the maintenance of aerobic life on earth. The production of oxygen occurs at the PSII oxygen-evolving complex (OEC), which contains a tetranuclear manganese (Mn) cluster. Photo-induced electron transfer events in the reaction center lead to the accumulation of oxidizing equivalents on the OEC. Four sequential photooxidation reactions are required for oxygen production. The oxidizing complex cycles among five oxidation states, called the S n states, where n refers to the number of oxidizing equivalents stored. Oxygen release occurs during the S 3-to-S0 transition from an unstable intermediate, known as the S4 state. In this report, we present data providing evidence for the production of an intermediate during each S state transition. These proteinderived intermediates are produced on the microsecond to millisecond time scale and are detected by time-resolved vibrational spectroscopy on the microsecond time scale. Our results suggest that a protein-derived conformational change or proton transfer reaction precedes Mn redox reactions during the S 2-to-S3 and S 3-to-S0 transitions.manganese cluster ͉ photosynthesis ͉ photosystem II ͉ time-resolved IR ͉ water oxidation T ime-resolved vibrational spectroscopy can detect chemical intermediates formed during enzymatic catalysis. Advantages include the technique's exquisite structural sensitivity and its high temporal resolution. Recent advances in methodology and interpretation have produced insights into the catalytic mechanism in several biological systems (for examples, see refs. 1-4).In this paper, we report the use of time-resolved IR spectroscopy to investigate the mechanism of photosynthetic water oxidation. Photosystem II (PSII) catalyzes the oxidation of water and the reduction of bound plastoquinone. Photoexcitation of PSII leads to the oxidation of the chlorophyll donor, P 680 , and the sequential reduction of a pheophytin (Fig. 1A, reaction 1) and a plastoquinone, Q A ( Fig. 1 A, reaction 2), in picoseconds. Q A reduces Q B to generate a semiquinone radical, Q B Ϫ , on the microsecond time scale (Fig. 1 A, reaction 3 ) (reviewed in ref. 5).A second photoexcitation leads to the reduction and protonation of Q B Ϫ to form the quinol Q B H 2 . The rate of reduction of Q B is faster than the rate of reduction of Q B Ϫ (see ref. 6 and references therein), which gives rise to a characteristic period-2 oscillation in kinetics originating on the PSII acceptor side (7).The primary chlorophyll donor, P 680 , oxidizes a tyrosine, Y Z (Y161 in the D1 subunit), on the nanosecond to microsecond time scale (Fig. 1 A, reaction 4). In turn, tyrosine Y Z ⅐ oxidizes the oxygen-evolving complex (OEC) on every flash (Fig. 1 A, reaction 5) (8). Four sequential photooxidation reactions are required for oxygen production, and the oxidizing complex cycles among five oxidation states, called the S n states, where n refers to the number of oxidizing equivalents stored (9). The rate of OEC oxidation slows as o...

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Section: Discussionmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Time-resolved vibrational spectroscopy detects protein-based intermediates in the photosynthetic oxygen-evolving cycle

Barry

Cooper²,

Riso³

et al. 2006

Proc. Natl. Acad. Sci. U.S.A.

Self Cite

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“…Reaction-induced FT-IR difference spectroscopy was performed at 263 K and pH 7.5, and in the presence of 7 mM potassium ferricyanide, as previously described (17,(46)(47)(48). The resuspended sample, described above, was thawed and pelleted.…”

Section: Methodsmentioning

confidence: 99%

A hydrogen-bonding network plays a catalytic role in photosynthetic oxygen evolution

Polander

Barry

2012

Proc. Natl. Acad. Sci. U.S.A.

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In photosystem II, oxygen evolution occurs by the accumulation of photo-induced oxidizing equivalents at the oxygen-evolving complex (OEC). The sequentially oxidized states are called the S 0 -S 4 states, and the dark stable state is S 1 . Hydrogen bonds to water form a network around the OEC; this network is predicted to involve multiple peptide carbonyl groups. In this work, we tested the idea that a network of hydrogen bonded water molecules plays a catalytic role in water oxidation. As probes, we used OEC peptide carbonyl frequencies, the substrate-based inhibitor, ammonia, and the sugar, trehalose. Reaction-induced FT-IR spectroscopy was used to describe the protein dynamics associated with the S 1 to S 2 transition. A shift in an amide CO vibrational frequency (1664 (S 1 ) to 1653 (S 2 ) cm −1 ) was observed, consistent with an increase in hydrogen bond strength when the OEC is oxidized. Treatment with ammonia/ammonium altered these CO vibrational frequencies. The ammonia-induced spectral changes are attributed to alterations in hydrogen bonding, when ammonia/ammonium is incorporated into the OEC hydrogen bond network. The ammonia-induced changes in CO frequency were reversed or blocked when trehalose was substituted for sucrose. This trehalose effect is attributed to a displacement of ammonia molecules from the hydrogen bond network. These results imply that ammonia, and by extension water, participate in a catalytically essential hydrogen bond network, which involves OEC peptide CO groups. Comparison to the ammonia transporter, AmtB, reveals structural similarities with the bound water network in the OEC.amide carbonyl frequency | Amt B transporter | photosystem II | vibrational spectroscopy | water oxidation I n oxygenic photosynthesis, photosystem II (PSII) catalyzes the oxidation of water and reduction of plastoquinone (1). Each reaction center includes the transmembrane subunits D1, D2, CP43, and CP47, which bind the redox-active cofactors. After photoexcitation, a charge separation is generated between the dimeric chl donor, P 680 , and a bound plastoquinone, Q A . Q A − reduces a second quinone, Q B , and P 680 þ oxidizes a tyrosine residue, YZ, Y161 in the D1 polypeptide. The radical, YZ•, is a powerful oxidant (2). Under physiological conditions, YZ• oxidizes the Mn 4 CaO 5 cluster, where water oxidation occurs (3). Four sequential photooxidations lead to the release of molecular oxygen (4). The oxygen yield fluctuates with period four. The sequentially oxidized states of the Mn cluster are called the Sn states, where n refers to the number of oxidizing equivalents stored at the OEC. S 1 is the dark stable state of the OEC. A single flash given to a dark-adapted sample of PSII generates the S 2 state, which corresponds to the oxidation of Mn(III) to Mn (IV) (5). The water oxidation chemistry in the S state cycle occurs on the microsecond to millisecond time scale, and oxygen is released during the S 3 to S 0 transition (4, 6).The structure of PSII has been reported at a resolution of 1.9 Å (3). T...

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“…On the assumption that Ca 2+ had been removed from its binding site without the use of a chelator, the modified spectral properties of the S 2 state have been attributed to binding of the chelator to the Ca 2+ -depleted Mn cluster (Boussac et al 1990;Kimura and Ono 2001). However, the implication that without chelator the Ca 2+ -free S 2 state would not be modified seems at odds with the fact that even replacement of Ca 2+ by Sr 2+ , which is so similar to Ca 2+ that it supports O 2 evolution, clearly modifies the EPR (Boussac and Rutherford 1988b) and FTIR (Barry et al 2005;DeRiso et al 2006) spectral properties of the S 2 state. Therefore, we prefer the direct interpretation that chelators prevent rebinding of Ca 2+ after NaCl/light treatment.…”

Section: Ca 2+ Depletion Methods Revisitedmentioning

confidence: 99%

The PSII calcium site revisited

2007

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Oxidation of H 2 O by photosystem II is a unique redox reaction in that it requires Ca 2+ as well as Cl -as obligatory activators/cofactors of the reaction, which is catalyzed by Mn atoms. The properties of the binding site for Ca 2+ in this reaction resemble those of other Ca 2+ binding proteins, and recent X-ray structural data confirm that the metal is in fact ligated at least in part by amino acid side chain oxo anions. Removal of Ca 2+ blocks water oxidation chemistry at an early stage in the cycle of redox reactions that result in O-O bond formation, and the intimate involvement of Ca 2+ in this reaction that is implied by this result is confirmed by an ever-improving set of crystal structures of the cyanobacterial enzyme. Here, we revisit the photosystem II Ca 2+ site, in part to discuss the additional information that has appeared since our earlier review of this subject (van Gorkom HJ, Yocum CF In: Wydrzynski TJ, Satoh K (eds) Photosystem II: the light-driven water:plastoquinone oxidoreductase), and also to reexamine earlier data, which lead us to conclude that all S-state transitions require Ca 2+ .

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Calcium Ligation in Photosystem II under Inhibiting Conditions

Cited by 18 publications

References 63 publications

Time-resolved vibrational spectroscopy detects protein-based intermediates in the photosynthetic oxygen-evolving cycle

Time-resolved vibrational spectroscopy detects protein-based intermediates in the photosynthetic oxygen-evolving cycle

A hydrogen-bonding network plays a catalytic role in photosynthetic oxygen evolution

The PSII calcium site revisited

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